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PMID: 11104784 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Inhibition of VEGF receptors causes lung cell apoptosis and emphysema.

The Journal of clinical investigation ·Vol. 106 ·No. 11 ·2000-12-00 ·Pages 1311-9

Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF

Abstract

Pulmonary emphysema, a significant global health problem, is characterized by a loss of alveolar structures. Because VEGF is a trophic factor required for the survival of endothelial cells and is abundantly expressed in the lung, we hypothesized that chronic blockade of VEGF receptors could induce alveolar cell apoptosis and emphysema. Chronic treatment of rats with the VEGF receptor blocker SU5416 led to enlargement of the air spaces, indicative of emphysema. The VEGF receptor inhibitor SU5416 induced alveolar septal cell apoptosis but did not inhibit lung cell proliferation. Viewed by angiography, SU5416-treated rat lungs showed a pruning of the pulmonary arterial tree, although we observed no lung infiltration by inflammatory cells or fibrosis. SU5416 treatment led to a decrease in lung expression of VEGF receptor 2 (VEGFR-2), phosphorylated VEGFR-2, and Akt-1 in the complex with VEGFR-2. Treatment with the caspase inhibitor Z-Asp-CH(2)-DCB prevented SU5416-induced septal cell apoptosis and emphysema development. These findings suggest that VEGF receptor signaling is required for maintenance of the alveolar structures and, further, that alveolar septal cell apoptosis contributes to the pathogenesis of emphysema.

MeSH Terms
Angiography Animals Apoptosis/drug effects Aspartic Acid/analogs & derivatives,pharmacology Caspase 3 Caspase Inhibitors Caspases/metabolism Cell Adhesion/drug effects Cells, Cultured Collagen DNA Fragmentation/drug effects Dose-Response Relationship, Drug Drug Combinations Enzyme Inhibitors/pharmacology Epithelial Cells/cytology,drug effects Immunohistochemistry In Situ Nick-End Labeling Indoles/pharmacology Laminin Lung/chemistry,drug effects,pathology Male Proliferating Cell Nuclear Antigen/metabolism Protease Inhibitors/pharmacology Proteoglycans Pulmonary Emphysema/diagnostic imaging,etiology,pathology Pyrroles/pharmacology Rats Rats, Sprague-Dawley Receptor Protein-Tyrosine Kinases/antagonists & inhibitors Receptors, Growth Factor/antagonists & inhibitors Receptors, Vascular Endothelial Growth Factor
Chemicals
Caspase Inhibitors Drug Combinations Enzyme Inhibitors Indoles Laminin Proliferating Cell Nuclear Antigen Protease Inhibitors Proteoglycans Pyrroles Receptors, Growth Factor benzyloxycarbonyl-Asp-CH2OC(O)-2,6-dichlorobenzene matrigel Aspartic Acid Semaxinib Collagen Receptor Protein-Tyrosine Kinases Receptors, Vascular Endothelial Growth Factor Casp3 protein, rat Caspase 3 Caspases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Kasahara Y
Division of Pulmonary Sciences and Critical Care Medicine, Pulmonary Hypertension Center, Department of Medicine, University of Colorado Health Sciences Center, Denver, USA.
Tuder R M
Taraseviciene-Stewart L
Le Cras T D
Abman S
Hirth P K
Waltenberger J
Voelkel N F
References (33)
33 references, click to expand
  1. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele.
    Nature. 1996 Apr 4;380(6573):435-9 PMID: 8602241
  2. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity.
    Nat Med. 1995 Oct;1(10):1024-8 PMID: 7489357
  3. Presence of double-strand breaks with single-base 3' overhangs in cells undergoing apoptosis but not necrosis.
    J Cell Biol. 1996 Dec;135(5):1369-76 PMID: 8947557
  4. Retinoic acid treatment abrogates elastase-induced pulmonary emphysema in rats.
    Nat Med. 1997 Jun;3(6):675-7 PMID: 9176496
  5. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice.
    Science. 1997 Sep 26;277(5334):2002-4 PMID: 9302297
  6. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells.
    J Biol Chem. 1998 May 22;273(21):13313-6 PMID: 9582377
  7. Homologous up-regulation of KDR/Flk-1 receptor expression by vascular endothelial growth factor in vitro.
    J Biol Chem. 1998 Nov 6;273(45):29979-85 PMID: 9792718
  8. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation.
    J Biol Chem. 1998 Nov 13;273(46):30336-43 PMID: 9804796
  9. Trafficking of newly synthesized surfactant protein A in isolated rat alveolar type II cells.
    Am J Respir Cell Mol Biol. 1998 Dec;19(6):929-35 PMID: 9843927
  10. Vascular endothelial growth factor (VEGF) and its receptors.
    FASEB J. 1999 Jan;13(1):9-22 PMID: 9872925
  11. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene.
    Nature. 1996 Apr 4;380(6573):439-42 PMID: 8602242
  12. In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system.
    Cell Death Differ. 1998 Dec;5(12):1004-16 PMID: 9894607
  13. VEGF is required for growth and survival in neonatal mice.
    Development. 1999 Mar;126(6):1149-59 PMID: 10021335
  14. Induction of apoptotic cell death in vascular endothelial cells cultured in three-dimensional collagen lattice.
    Exp Cell Res. 1999 May 1;248(2):498-508 PMID: 10222141
  15. Abnormal lung growth and the development of pulmonary hypertension in the Fawn-Hooded rat.
    Am J Physiol. 1999 Oct;277(4 Pt 1):L709-18 PMID: 10516211
  16. The bronchial arteries in pulmonary emphysema.
    Thorax. 1953 Mar;8(1):46-58 PMID: 13038737
  17. Pulmonary emphysema with special reference to vascular changes.
    Am Rev Respir Dis. 1959 Jul;80(1, Part 2):67-93 PMID: 13670406
  18. Antiangiogenic therapy targeting the tyrosine kinase receptor for vascular endothelial growth factor receptor inhibits the growth of colon cancer liver metastasis and induces tumor and endothelial cell apoptosis.
    Cancer Res. 1999 Nov 1;59(21):5412-6 PMID: 10554007
  19. Animal models for chronic obstructive pulmonary disease: age of klotho and marlboro mice.
    Am J Respir Cell Mol Biol. 2000 Jan;22(1):4-7 PMID: 10615058
  20. SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types.
    Cancer Res. 1999 Jan 1;59(1):99-106 PMID: 9892193
  21. Disruption of the klotho gene causes pulmonary emphysema in mice. Defect in maintenance of pulmonary integrity during postnatal life.
    Am J Respir Cell Mol Biol. 2000 Jan;22(1):26-33 PMID: 10615062
  22. Regulation of vascular growth and regression by matrix metalloproteinases in the rat aorta model of angiogenesis.
    Lab Invest. 2000 Apr;80(4):545-55 PMID: 10780671
  23. Inhibition of angiogenesis decreases alveolarization in the developing rat lung.
    Am J Physiol Lung Cell Mol Physiol. 2000 Sep;279(3):L600-7 PMID: 10956636
  24. Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema.
    Am J Respir Crit Care Med. 2001 Mar;163(3 Pt 1):737-44 PMID: 11254533
  25. Studies in alpha 1-antitrypsin deficiency.
    Acta Med Scand Suppl. 1965;432:1-85 PMID: 4160491
  26. Measurement of pulmonary emphysema.
    Am Rev Respir Dis. 1967 May;95(5):752-64 PMID: 5337140
  27. Newer aspects of the pulmonary vasculature in chronic lung disease. A comparative study.
    Angiology. 1968 Jul-Aug;19(7):399-407 PMID: 5664335
  28. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid.
    Science. 1983 Feb 25;219(4587):983-5 PMID: 6823562
  29. Detection of antileukoprotease in connective tissue of the lung.
    Histochemistry. 1986;86(2):165-8 PMID: 2434453
  30. Chronic obstructive pulmonary disease: a definition and implications of structural determinants of airflow obstruction for epidemiology.
    Am Rev Respir Dis. 1989 Sep;140(3 Pt 2):S3-8 PMID: 2675711
  31. Agarose infiltration improves morphology of cryostat sections of lung.
    Lab Invest. 1994 Jul;71(1):149-53 PMID: 7518881
  32. Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide.
    J Clin Invest. 1995 Apr;95(4):1798-807 PMID: 7706486
  33. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. American Thoracic Society.
    Am J Respir Crit Care Med. 1995 Nov;152(5 Pt 2):S77-121 PMID: 7582322
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2000-12-00
Pages
1311-9
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC387249
Subset
IM
Grants
NHLBI NIH HHS · R01 HL066554 · United States
NHLBI NIH HHS · 1RO1 HL60195-01 · United States
NHLBI NIH HHS · 1RO1 HL60913-01 · United States
NHLBI NIH HHS · 1RO1 HL66554-01 · United States
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